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Genetic Manipulation of the Brassicaceae Smut Fungus Thecaphora Thlaspeos

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Genetic Manipulation of the Brassicaceae Smut Fungus Thecaphora Thlaspeos Journal of Fungi Article Genetic Manipulation of the Brassicaceae Smut Fungus Thecaphora thlaspeos Lesley Plücker †, Kristin Bösch †, Lea Geißl, Philipp Hoffmann and Vera Göhre * Institute of Microbiology, Cluster of Excellence in Plant Sciences, Heinrich-Heine University, Building 26.24.01, Universitätsstr.1, 40205 Düsseldorf, Germany; [email protected] (L.P.); [email protected] (K.B.); [email protected] (L.G.); [email protected] (P.H.) * Correspondence: [email protected]; Tel.: +49-211-811-1529 † These authors contribute equally to this work. Abstract: Investigation of plant–microbe interactions greatly benefit from genetically tractable part- ners to address, molecularly, the virulence and defense mechanisms. The smut fungus Ustilago maydis is a model pathogen in that sense: efficient homologous recombination and a small genome allow targeted modification. On the host side, maize is limiting with regard to rapid genetic alterations. By contrast, the model plant Arabidopsis thaliana is an excellent model with a vast amount of information and techniques as well as genetic resources. Here, we present a transformation protocol for the Brassicaceae smut fungus Thecaphora thlaspeos. Using the well-established methodology of protoplast transformation, we generated the first reporter strains expressing fluorescent proteins to follow mating. As a proof-of-principle for homologous recombination, we deleted the pheromone receptor pra1. As expected, this mutant cannot mate. Further analysis will contribute to our understanding of the role of mating for infection biology in this novel model fungus. From now on, the genetic manipulation of T. thlaspeos, which is able to colonize the model plant A. thaliana, provides us with a pathosystem in which both partners are genetically amenable to study smut infection biology. Keywords: mating; pheromone receptor; homologous recombination; infection; smut; transforma- tion; protoplast Citation: Plücker, L.; Bösch, K.; Geißl, L.; Hoffmann, P.; Göhre, V. Genetic Manipulation of the Brassicaceae Smut Fungus Thecaphora 1. Introduction thlaspeos. J. Fungi 2021, 7, 38. https://doi.org/10.3390/jof7010038 Smut fungi are important pathogens causing economic losses in crops such as barley, wheat, maize, and potato [1]. The dimorphic lifecycle of grass smut fungi is comprised Received: 16 November 2020 of a yeast form [2] that, in contrast to many other biotrophic fungi, can be cultured, and Accepted: 7 January 2021 is amenable to genetic manipulation [3]. In combination with the efficient homologous Published: 9 January 2021 recombination, this has turned Ustilago maydis, the maize smut fungus [4], into an important model organism for fungal and infection biology [5,6]. Publisher’s Note: MDPI stays neu- U. maydis starts the infection by mating, resulting in the morphological switch to tral with regard to jurisdictional clai- the infectious filamentous form. Mating in smut fungi is controlled by two mating loci. ms in published maps and institutio- The a locus encodes for pheromones (mfa) and pheromone receptors (pra) that mediate nal affiliations. recognition of compatible mating partners and trigger cell fusion [7]. The b locus contains two genes (bW, bE) encoding for subunits of a heterodimeric, homeodomain transcription factor. When an active transcription factor is assembled from different alleles in the common cytosol after plasmogamy, filamentous growth is initiated and thereby the fungus switches Copyright: © 2021 by the authors. Li- censee MDPI, Basel, Switzerland. from saprophytic to pathogenic growth [8]. Notably, the infectious filaments are arrested This article is an open access article in the cell cycle until successful penetration of the host plant [9]. This mating system is distributed under the terms and con- widely conserved in grass smut fungi and allows for genetic exchange between the mating ditions of the Creative Commons At- partners [10]. tribution (CC BY) license (https:// In contrast to the well-characterized grass smut fungi infecting important monocot creativecommons.org/licenses/by/ crop plants with U. maydis at the forefront, little is known about smut fungi infecting 4.0/). dicot plants. A reemerging example is Microbotryum that is regaining attention today [11]. J. Fungi 2021, 7, 38. https://doi.org/10.3390/jof7010038 https://www.mdpi.com/journal/jof J. Fungi 2021, 7, 38 2 of 14 By contrast, the Thecaphora-clade [12], with agronomically relevant members such as T. solani [13] or T. frezii [14] infecting potato and peanut, respectively, remains largely elusive. One member, the Brassicaceae smut fungus T. thlaspeos, infects several Arabis species [12] and can colonize Arabidopsis thaliana [15], making it a good system to study smut infection in model plants. Interestingly, germinating teliospores of T. thlaspeos directly give rise to an infectious filament, and no saprophytic phase is known. However, prolonged cultivation leads to fungal proliferation as filamentous, haploid cultures. From such cultures, two filamentous haploid T. thlaspeos strains of compatible mating types, LF1 and LF2, could be isolated [15]. The unique germination pattern and the emergence of haploid filaments in culture raise questions about mating and meiosis in T. thlaspeos. The genome of T. thlaspeos was recently sequenced and annotated. With 20.5 Mb, 6239 gene models, and a low repeat content, it is a typical smut fungal genome [16]. Notably, we could identify the mating loci a and b in this genome. In comparison to the grass smut fungi, the a locus of T. thlaspeos is strongly rearranged, and aligns well to the biocontrol yeast Anthracocystis flocculosa (formerly Pseudozyma flocculosa). It still contains one copy of the pheromone receptor pra1 and pheromone mfa1, or pra2 and mfa2 in T. thlaspeos LF1 and LF2, respectively [16]. The b locus is conserved with a bi-directional promoter in between the two genes, and we have previously shown that the heterodimer formation of bE and bW isconserved in T. thlaspeos [15]. Conservation of the mating genes throughout evolution suggests that T. thlaspeos still uses mating, e.g., for exchange of genetic material. However, the infectious lifecycle so far has not revealed a stage where mating is required. Therefore, we aimed for a more detailed understanding of the role of the T. thlaspeos mating genes. To study the mating process in T. thlaspeos, genetic manipulation is essential. For example, reporter lines enable life-cell imaging, and deletion mutants can give insight into mutant phenotypes. Several transformation methods have been developed for smut fungi. Protoplast-mediated transformation is used for the grass smuts U. maydis [17], Sporisorium reilianum [18], U. hordei [19], U. esculenta [20], and U. bromivora [21], as well as the filamentous Basidiomycete Serendipita indica (formerly Piriformospora indica)[22], and the biocontrol yeast An. flocculosa [23]. Agrobacterium-mediated transformation is used for S. scitamineum in combination with a CRISPR-Cas9 system [24], and also for bringing larger fragments into U. hordei [25] and for gene tagging in U. maydis [26]. Here, we have established a protoplast-based PEG-mediated transformation system and generated targeted deletion mutants to investigate the mating process in T. thlaspeos. 2. Materials and Methods 2.1. Fungal Culture Conditions T. thlaspeos LF1 and LF2 haploid strains [15] from our own collection were used in this study. Both were grown in YEPS light liquid medium (1% yeast extract w/v, 0.4% w/v Bacto TM-Peptone, and 0.4% w/v sucrose) or YEPS light solid medium with 0.6% w/v plant agar or 1% w/v phytagel at 18 ◦C. Cryostocks of T. thlaspeos were generated by mixing exponentially growing cultures with 30% glycerol in growth medium followed by immediate freezing at −80 ◦C. Filamentous cultures were started by resuspending the glycerol stock in growth medium or plating the cells on solid medium as described above. 2.2. Plasmid Construction All plasmids used in this study were generated with the Golden Gate Cloning tech- nique (Protocol S1) as described [27]. The hpt-egfp and hpt-mcherry sequences were codon- optimized for U. maydis. Promoter and terminator sequences from T. thlaspeos or U. maydis were amplified via PCR from genomic DNA. 2.3. Protoplasting T. thlaspeos cultures were grown in YEPS light medium to an OD600 of 0.5–0.8 for 3 to 4 days. Fungal mycelium was collected using cell strainers with 40 µm mesh size (VWR TM Darmstadt, Germany) and washed with protoplasting buffer (0.1 M sodium citrate, 0.01 M J. Fungi 2021, 7, 38 3 of 14 EDTA 1.2 M MgSO4, and pH 5.8) to remove residual culture medium. T. thlaspeos tissue was resuspended in 9 mL protoplasting buffer, supplemented with 10 mg/mL Yatalase (Takara Bio, Kusatsu, Japan) and 20 mg/mL Glucanex (Sigma-Aldrich, St. Luis, MI, USA) per 100 mL cell culture, and incubated for 30–60 min at room temperature. Protoplast formation was controlled microscopically. When protoplasting was finished, protoplasting buffer was added to a total volume of 24 mL. Aliquots of 6 mL crude protoplast solution were overlayed with 5 mL trapping buffer (0.6 M sorbitol, 0.1 M Tris/HCl pH 7.0) and centrifuged at 4863× g (5000 rpm) in a swing out rotor at 4 ◦C for 15 min. The interphase was collected from all tubes and diluted with 2 volumes of ice-cold STC buffer (0.01 M Tris/HCl pH 7.5, 0.1 M CaCl2, and 1.0 M sorbitol). Protoplasts were pelleted at 4863× g (5000 rpm) in a swing out rotor at 4 ◦C for 10 min and resuspended in 500 µL ice-cold STC buffer. 100 µL protoplast aliquots were used for transformation immediately. A bullet point version of the protocol is available with the supplementary files (Protocol S1). 2.4. Transformation Transformation of T. thlaspeos protoplasts were carried out as described for U. may- dis [28] with slight modifications. Transformation reactions were spread on YMPG-Reg (0.3% w/v Yeast extract, 0.3% w/v malt extract, 0.5% w/v Bacto-Peptone, 1% w/v glucose, 1 M sucrose, 0.6% w/v plant agar, Duchefa Biochemie, Haarlem, Netherlands) medium and incubated at 18 ◦C until colonies appeared (1–2 months).
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